Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI

Recent studies in both monkeys and humans indicate that the dorsal premotor cortex participates in spatial attention and working memory, in addition to its well known role in movement planning and execution. One important question is whether these functions overlap or are segregated within this frontal area. Single-cell recordings in monkeys suggest a relative specialization of the rostral portion of dorsal premotor cortex for attention and/or memory and of the caudal region for motor preparation. To test whether this possibility also holds true in humans, we used functional magnetic resonance imaging (fMRI) to compare, in the same set of subjects, brain activation related to strong spatial attention and memory demands to that elicited by long motor preparatory periods. The behavioral protocol was based on a task that had proved effective for dissociating neuronal properties related to these two functions in the monkey brain. The principle of the monkey task was that a first cue guided the focus of spatial attention and memory, whereas a second one instructed an arm movement. Based on this principle, two tasks were developed. One maximized spatial attention and memory demands by presenting long series of stimuli (4, 8, or 12) before the motor instructional cue, whereas the other extended the motor preparation phase by imposing long and variable delays (1-5.5 s) between the onset of the instructional cue and movement execution. The two tasks and their respective control conditions were arranged in two blocked-design sequences. The results indicate that the brain networks underlying the two functional domains overlap in the caudate nucleus and presupplementary motor area, and possibly in lateral prefrontal cortex as well, but involve different dorsal premotor fields. Motor preparation primarily recruited a dorsal premotor area located caudally, within the precentral gyrus (together with the supplementary motor area), whereas spatial attention and memory preferentially activated a more rostral site, in and anterior to the precentral sulcus (in addition to the posterior parietal cortex). These findings strengthen the idea that the primate dorsal premotor cortex contributes to both motor and nonmotor processes. Moreover, they corroborate emerging evidence from monkey physiology suggesting a relative functional segregation within this cortex, with attention to short-term storage of visuospatial information engaging a more rostral region than motor preparation.